Microtubules originate asymmetrically at the somatic Golgi and are guided via Kinesin2 to maintain polarity in neurons

  1. Amrita Mukherjee
  2. Paul S Brooks
  3. Fred Bernard
  4. Antoine Guichet
  5. Paul T Conduit  Is a corresponding author
  1. University of Cambridge, United Kingdom
  2. Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, France

Abstract

Neurons contain polarised microtubule arrays essential for neuronal function. How microtubule nucleation and polarity are regulated within neurons remains unclear. We show that γ-tubulin localises asymmetrically to the somatic Golgi within Drosophila neurons. Microtubules originate from the Golgi with an initial growth preference towards the axon. Their growing plus ends also turn towards and into the axon, adding to the plus-end-out microtubule pool. Any plus ends that reach a dendrite, however, do not readily enter, maintaining minus-end-out polarity. Both turning towards the axon and exclusion from dendrites depend on Kinesin-2, a plus-end-associated motor that guides growing plus ends along adjacent microtubules. We propose that Kinesin-2 engages with a polarised microtubule network within the soma to guide growing microtubules towards the axon; while at dendrite entry sites engagement with microtubules of opposite polarity generates a backward stalling force that prevents entry into dendrites and thus maintains minus-end-out polarity within proximal dendrites.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figure 6 and 7.

Article and author information

Author details

  1. Amrita Mukherjee

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Paul S Brooks

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Fred Bernard

    Polarity and Morphogenesis Lab, Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7919-253X
  4. Antoine Guichet

    Polarity and Morphogenesis Lab, Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7216-1944
  5. Paul T Conduit

    Department of Zoology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    ptc29@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7822-1191

Funding

Wellcome (105653/Z/14/Z)

  • Amrita Mukherjee
  • Paul S Brooks
  • Paul T Conduit

Isaac Newton Trust (18.23(p))

  • Amrita Mukherjee
  • Paul T Conduit

Association pour la Recherche sur le Cancer (PJA 20181208148)

  • Fred Bernard
  • Antoine Guichet

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2020, Mukherjee et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Amrita Mukherjee
  2. Paul S Brooks
  3. Fred Bernard
  4. Antoine Guichet
  5. Paul T Conduit
(2020)
Microtubules originate asymmetrically at the somatic Golgi and are guided via Kinesin2 to maintain polarity in neurons
eLife 9:e58943.
https://doi.org/10.7554/eLife.58943

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https://doi.org/10.7554/eLife.58943